Multilevel atlas comparisons reveal divergent evolution of the primate brain

Abstract

Whether the size of the prefrontal cortex (PFC) in humans is disproportionate when compared to other species is a persistent debate in evolutionary neuroscience. This question has left the study of over/under-expansion in other structures relatively unexplored. We therefore sought to address this gap by adapting anatomical areas from the digital atlases of 18 mammalian species, to create a common interspecies classification. Our approach used data-driven analysis based on phylogenetic generalized least squares to evaluate anatomical expansion covering the whole brain. Our main finding suggests a divergence in primate evolution, orienting the stereotypical mammalian cerebral proportion toward a frontal and parietal lobe expansion in catarrhini (primate parvorder comprising old world monkeys, apes, and humans). Cerebral lobe volumes slopes plotted for catarrhini species were ranked as parietal∼frontal > temporal > occipital, contrasting with the ranking of other mammalian species (occipital > temporal > frontal∼parietal). Frontal and parietal slopes were statistically different in catarrhini when compared to other species through bootstrap analysis. Within the catarrhini’s frontal lobe, the prefrontal cortex was the principal driver of frontal expansion. Across all species, expansion of the frontal lobe appeared to be systematically linked to the parietal lobe. Our findings suggest that the human frontal and parietal lobes are not disproportionately enlarged when compared to other catarrhini. Nevertheless, humans remain unique in carrying the most relatively enlarged frontal and parietal lobes in an infraorder exhibiting a disproportionate expansion of these areas.